Download PDF
Am J Perinatol 2020; 37(11): 1160-1172
DOI: 10.1055/s-0039-1692715
Original Article

Exploration of the Vaginal and Gut Microbiome in African American Women by Body Mass Index, Class of Obesity, and Gestational Weight Gain: A Pilot Study

Mary Ann Faucher 
1   Louise Herrington School of Nursing, Midwifery Specialty, Baylor University, Dallas, Texas
,
Kristen Leigh Greathouse
2   Department of Nutrition Science, Baylor University, Waco, Texas
,
Marie Hastings-Tolsma
1   Louise Herrington School of Nursing, Midwifery Specialty, Baylor University, Dallas, Texas
,
Robert Noah Padgett
3   Department of Educational Psychology, Baylor University, Waco, Texas
,
Kimberly Sakovich
4   Women's Health Care, MacArthur Obstetrics and Gynecology, Irving, Texas
,
Ankan Choudhury
5   Department of Biology, Baylor University, Waco, Texas
,
Aadil Sheikh
5   Department of Biology, Baylor University, Waco, Texas
,
Nadim J. Ajami
6   Department of Molecular Virology and Microbiology, Baylor College of Medicine, Texas Medical Center, Houston, Texas
,
Joseph F. Petrosino
7   The Alkek Center for Metagenomics and Microbiome Research, Baylor College of Medicine, Texas Medical Center, Houston, Texas
› Author Affiliations Funding This study was funded by the Collaborative Faculty Research Innovation Program (CFRIP) grant from Baylor University, Baylor College of Medicine, and Baylor Research Institution-Project number 30300146.
› Further Information
Also available at
    Permissions and Reprints

Abstract

Objective This study determines the differences in the distal gut and vaginal microbiome in African American (AA) women by prepregnancy body mass index and gestational weight gain (GWG) comparing women with and without obesity and by obesity class.

Study Design We prospectively sampled the vaginal and distal gut microbiome in pregnant AA women at two time points during pregnancy. Samples were analyzed using high-throughput sequencing of the V4 region of the 16S ribosomal ribonucleic acid gene.

Results Distinct differences in vaginal and distal gut α-diversity were observed at time point 1 between women with and without obesity by total GWG. Significant differences in distal gut β-diversity were also found at time point 1 in obese women by GWG. Within the Bacteroides genus, a significant association was observed by total GWG among obese women which was absent in nonobese women. Women with class III obesity who experienced low GWG had the lowest abundance of distal gut Bacteroides and appreciably higher relative abundance of a consortia of vaginal taxa including Atopobium, Gardnerella, Prevotella, and Sneathia.

Conclusion These results contribute new evidence showing that GWG in combination with obesity and obesity class is associated with an altered distal gut and vaginal composition early in pregnancy among AA women.

Keywords

gestational weight gain - obesity - obesity class - microbiome - African American - pregnancy

Declaration of Data Set

The data set supporting the conclusions of this article included within the article and its' additional files is available in the BioProject database/ repository, BioProject ID: PRJNA422447, link: https://urldefense.proofpoint.com/v2/url?u=http-3A__www.ncbi.nlm.nih.gov_bioproject_422447&d=DwICaQ&c=ZQs-KZ8oxEw0p81sqgiaRA&r=YTUxyBdU_6BctUsXVw5ZzwpbWswno7FbIZTkWuuKt1s&m=uyeGLBv-Cc4pPpaIxdDJJD_q_5mZCJm0YtPkeYRPCVg&s=urOK5llZoIIt2FtH9WZjPyIJdc6PassC4uGkIJumozM&e=.


Authors' Contributions

M.A.F., K.L.G., M.H.T., K.S., N.A., and J.P. have taken part in the study design. M.A.F., K.L.G., M.H.T., A.C., A.S., N.A., R.N.P., and J.P. have contributed to the interpretation of the data, manuscript preparation, and/or review and approval of the final version. M.A.F. conceived the study design. M.A.F., M.H.T., and K.S. collected samples.


Supplementary Material



Publication History

Received: 28 January 2019

Accepted: 14 May 2019

Article published online:
26 June 2019

© 2020. Thieme. All rights reserved.

Thieme Medical Publishers
333 Seventh Avenue, New York, NY 10001, USA.

 

  • References

  • 1 Institute of Medicine [IOM]. Weight Gain during Pregnancy: Reexamining the Guidelines. Washington, DC: National Academies Press; 2009
    Search in Google Scholar
  • 2 Lutsiv O, Mah J, Beyene J, McDonald SD. The effects of morbid obesity on maternal and neonatal health outcomes: a systematic review and meta-analyses. Obes Rev 2015; 16 (07) 531-546
    CrossrefPubMedSearch in Google Scholar
  • 3 Faucher MA, Barger MK. Gestational weight gain in obese women by class of obesity and select maternal/newborn outcomes: A systematic review. Women Birth 2015; 28 (03) e70-e79
    CrossrefPubMedSearch in Google Scholar
  • 4 U.S. Department of Health and Human Services, Office of Minority Health. Obesity and African Americans. Available at: https://minorityhealth.hhs.gov/omh/browse.aspx?lvl=4&lvlid=25 . Accessed January 7, 2019
    PubMed
  • 5 Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 2014; 311 (08) 806-814
    CrossrefPubMedSearch in Google Scholar
  • 6 Cnattingius S, Villamor E, Johansson S. , et al. Maternal obesity and risk of preterm delivery. JAMA 2013; 309 (22) 2362-2370
    CrossrefPubMedSearch in Google Scholar
  • 7 Gillespie SL, Christian LM. Body mass index as a measure of obesity: racial differences in predictive value for health parameters during pregnancy. J Womens Health (Larchmt) 2016; 25 (12) 1210-1218
    CrossrefPubMedSearch in Google Scholar
  • 8 Sturm R, Hattori A. Morbid obesity rates continue to rise rapidly in the United States. Int J Obes 2013; 37 (06) 889-891
    CrossrefPubMedSearch in Google Scholar
  • 9 Koren O, Goodrich JK, Cullender TC. , et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 2012; 150 (03) 470-480
    CrossrefPubMedSearch in Google Scholar
  • 10 Nelson DB, Shin H, Wu J, Dominguez-Bello MG. The gestational vaginal microbiome and spontaneous preterm birth among nulliparous African American women. Am J Perinatol 2016; 33 (09) 887-893
    Thieme ConnectPubMedSearch in Google Scholar
  • 11 DiGiulio DB, Stevenson DK, Shaw G, Lyell DJ, Relman DA. Reply to Keelan and Payne: microbiota-related pathways for preterm birth. Proc Natl Acad Sci U S A 2015; 112 (47) E6415
    CrossrefPubMedSearch in Google Scholar
  • 12 Zhou X, Bent SJ, Schneider MG, Davis CC, Islam MR, Forney LJ. Characterization of vaginal microbial communities in adult healthy women using cultivation-independent methods. Microbiology 2004; 150 (Pt 8): 2565-2573
    CrossrefPubMedSearch in Google Scholar
  • 13 Hinkle SN, Sharma AJ, Dietz PM. Gestational weight gain in obese mothers and associations with fetal growth. Am J Clin Nutr 2010; 92 (03) 644-651
    CrossrefPubMedSearch in Google Scholar
  • 14 Collado MC, Isolauri E, Laitinen K, Salminen S. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr 2008; 88 (04) 894-899
    CrossrefPubMedSearch in Google Scholar
  • 15 Turnbaugh PJ, Hamady M, Yatsunenko T. , et al. A core gut microbiome in obese and lean twins. Nature 2009; 457 (7228): 480-484
    CrossrefPubMedSearch in Google Scholar
  • 16 Wen L, Duffy A. Factors influencing the gut microbiota, inflammation, and type 2 diabetes. J Nutr 2017; 147 (07) 1468S-1475S
    CrossrefPubMedSearch in Google Scholar
  • 17 Fettweis JM, Brooks JP, Serrano MG. , et al; The Vaginal Microbiome Consortium. Differences in vaginal microbiome in African American women versus women of European ancestry. Microbiology 2014; 160 (Pt 10): 2272-2282
    CrossrefPubMedSearch in Google Scholar
  • 18 DiGiulio DB, Callahan BJ, McMurdie PJ. , et al. Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci U S A 2015; 112 (35) 11060-11065
    CrossrefPubMedSearch in Google Scholar
  • 19 Romero R, Hassan SS, Gajer P. , et al. The vaginal microbiota of pregnant women who subsequently have spontaneous preterm labor and delivery and those with a normal delivery at term. Microbiome 2014; 2: 18
    CrossrefPubMedSearch in Google Scholar
  • 20 Stanislawski MA, Dabelea D, Wagner BD. , et al. Gut microbiota in the first 2 years of life and the association with body mass index at age 12 in a Norwegian birth cohort. MBio 2018; 9 (05) e01751-18
    CrossrefPubMedSearch in Google Scholar
  • 21 Goodrich JK, Waters JL, Poole AC. , et al. Human genetics shape the gut microbiome. Cell 2014; 159 (04) 789-799
    CrossrefPubMedSearch in Google Scholar
  • 22 Denison FC, Roberts KA, Barr SM, Norman JE. Obesity, pregnancy, inflammation, and vascular function. Reproduction 2010; 140 (03) 373-385
    CrossrefPubMedSearch in Google Scholar
  • 23 Budding AE, Grasman ME, Eck A. , et al. Rectal swabs for analysis of the intestinal microbiota. PLoS One 2014; 9 (07) e101344
    CrossrefPubMedSearch in Google Scholar
  • 24 Integrative HMP (iHMP) Research Network Consortium. The Integrative Human Microbiome Project: dynamic analysis of microbiome-host omics profiles during periods of human health and disease. Cell Host Microbe 2014; 16 (03) 276-289
    CrossrefPubMedSearch in Google Scholar
  • 25 Buffington SA, Di Prisco GV, Auchtung TA, Ajami NJ, Petrosino JF, Costa-Mattioli M. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 2016; 165 (07) 1762-1775
    CrossrefPubMedSearch in Google Scholar
  • 26 Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26 (19) 2460-2461
    CrossrefPubMedSearch in Google Scholar
  • 27 Quast C, Pruesse E, Yilmaz P. , et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013; 41 (Database issue): D590-D596
    CrossrefPubMedSearch in Google Scholar
  • 28 Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 2013; 10 (10) 996-998
    CrossrefPubMedSearch in Google Scholar
  • 29 Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005; 71 (12) 8228-8235
    CrossrefPubMedSearch in Google Scholar
  • 30 Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 2016; 13 (07) 581-583
    CrossrefPubMedSearch in Google Scholar
  • 31 World Health Organization [WHO]. Body Mass Index – BMI. Available at: http://www.euro.who.int/en/health-topics/disease-prevention/nutrition/a-healthy-lifestyle/body-mass-index-bmi . Accessed January 7, 2019
    PubMed
  • 32 Nelson DB, Hanlon AL, Wu G, Liu C, Fredricks DN. First trimester levels of BV-associated bacteria and risk of miscarriage among women early in pregnancy. Matern Child Health J 2015; 19 (12) 2682-2687
    CrossrefPubMedSearch in Google Scholar
  • 33 Aagaard K, Riehle K, Ma J. , et al. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One 2012; 7 (06) e36466
    CrossrefPubMedSearch in Google Scholar
  • 34 Smid MC, Ricks NM, Panzer A. , et al. Maternal gut microbiome biodiversity in pregnancy. Am J Perinatol 2018; 35 (01) 24-30
    Thieme ConnectPubMedSearch in Google Scholar
  • 35 Bisanz JE, Enos MK, PrayGod G. , et al. Microbiota at multiple body sites during pregnancy in a rural Tanzanian population and effects of moringa-supplemented probiotic yogurt. Appl Environ Microbiol 2015; 81 (15) 4965-4975
    CrossrefPubMedSearch in Google Scholar
  • 36 Gomez-Arango LF, Barrett HL, McIntyre HD, Callaway LK, Morrison M, Dekker Nitert M. SPRING Trial Group. Connections between the gut microbiome and metabolic hormones in early pregnancy in overweight and obese women. Diabetes 2016; 65 (08) 2214-2223
    CrossrefPubMedSearch in Google Scholar
  • 37 Carnero AM, Mejía CR, García PJ. Rate of gestational weight gain, pre-pregnancy body mass index and preterm birth subtypes: a retrospective cohort study from Peru. BJOG 2012; 119 (08) 924-935
    CrossrefPubMedSearch in Google Scholar
  • 38 Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444 (7122): 1027-1031
    CrossrefPubMedSearch in Google Scholar
  • 39 Bäckhed F, Ding H, Wang T. , et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 2004; 101 (44) 15718-15723
    CrossrefPubMedSearch in Google Scholar
  • 40 Sze MA, Schloss PD. Looking for a signal in the noise: revisiting obesity and the microbiome. MBio 2016; 7 (04) e01018-16
    CrossrefPubMedSearch in Google Scholar
  • 41 Ferrocino I, Ponzo V, Gambino R. , et al. Changes in the gut microbiota composition during pregnancy in patients with gestational diabetes mellitus (GDM). Sci Rep 2018; 8 (01) 12216
    CrossrefPubMedSearch in Google Scholar
  • 42 Hyman RW, Fukushima M, Jiang H. , et al. Diversity of the vaginal microbiome correlates with preterm birth. Reprod Sci 2014; 21 (01) 32-40
    CrossrefPubMedSearch in Google Scholar
  • 43 Antony KM, Ma J, Mitchell KB, Racusin DA, Versalovic J, Aagaard K. The preterm placental microbiome varies in association with excess maternal gestational weight gain. Am J Obstet Gynecol 2015; 212 (05) 653.e1-653.e16
    CrossrefPubMedSearch in Google Scholar
  • 44 Coyte KZ, Schluter J, Foster KR. The ecology of the microbiome: Networks, competition, and stability. Science 2015; 350 (6261): 663-666
    CrossrefPubMedSearch in Google Scholar
  • 45 Mendes-Soares H, Mundy M, Soares LM, Chia N. MMinte: an application for predicting metabolic interactions among the microbial species in a community. BMC Bioinformatics 2016; 17 (01) 343
    CrossrefPubMedSearch in Google Scholar
  • 46 Zhou X, Brown CJ, Abdo Z. , et al. Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J 2007; 1 (02) 121-133
    CrossrefPubMedSearch in Google Scholar
  • 47 Stout MJ, Zhou Y, Wylie KM, Tarr PI, Macones GA, Tuuli MG. Early pregnancy vaginal microbiome trends and preterm birth. Am J Obstet Gynecol 2017; 217 (03) 356.e1-356.e18
    CrossrefPubMedSearch in Google Scholar
  • 48 Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 2017; 11 (12) 2639-2643
    CrossrefPubMedSearch in Google Scholar
  • 49 Ravel J, Gajer P, Abdo Z. , et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 2011; 108 (Suppl. 01) 4680-4687
    CrossrefPubMedSearch in Google Scholar
  • 50 Ventolini G, Khandelwal N, Hutton K, Lugo J, Gygax SE, Schlabritz-Loutsevitch N. Obesity and recurrent vulvovaginal bacterial infections in women of reproductive age. Postgrad Med J 2017; 93 (1099): 297
    CrossrefPubMedSearch in Google Scholar
  • 51 Nelson DB, Hanlon A, Hassan S. , et al. Preterm labor and bacterial vaginosis-associated bacteria among urban women. J Perinat Med 2009; 37 (02) 130-134
    CrossrefPubMedSearch in Google Scholar
  • 52 Menard JP, Mazouni C, Salem-Cherif I. , et al. High vaginal concentrations of Atopobium vaginae and Gardnerella vaginalis in women undergoing preterm labor. Obstet Gynecol 2010; 115 (01) 134-140
    CrossrefPubMedSearch in Google Scholar
  • 53 Goldstein RF, Abell SK, Ranasinha S. , et al. Association of gestational weight gain with maternal and infant outcomes: a systematic review and meta-analysis. JAMA 2017; 317 (21) 2207-2225
    CrossrefPubMedSearch in Google Scholar
  • 54 Cerdó T, Ruiz A, Jáuregui R. , et al. Maternal obesity is associated with gut microbial metabolic potential in offspring during infancy. J Physiol Biochem 2018; 74 (01) 159-169
    CrossrefPubMedSearch in Google Scholar
  • 55 Baumann-Dudenhoeffer AM, D'Souza AW, Tarr PI, Warner BB, Dantas G. Infant diet and maternal gestational weight gain predict early metabolic maturation of gut microbiomes. Nat Med 2018; 24 (12) 1822-1829
    CrossrefPubMedSearch in Google Scholar
  • 56 Robinson A, Fiechtner L, Roche B. , et al. Association of maternal gestational weight gain with the infant fecal microbiota. J Pediatr Gastroenterol Nutr 2017; 65 (05) 509-515
    CrossrefPubMedSearch in Google Scholar
  • 57 Cedergren M. Effects of gestational weight gain and body mass index on obstetric outcome in Sweden. Int J Gynaecol Obstet 2006; 93 (03) 269-274
    CrossrefPubMedSearch in Google Scholar
  • 58 Bogaerts A, Ameye L, Martens E, Devlieger R. Weight loss in obese pregnant women and risk for adverse perinatal outcomes. Obstet Gynecol 2015; 125 (03) 566-575
    CrossrefPubMedSearch in Google Scholar
  • 59 Bodnar LM, Pugh SJ, Lash TL. , et al. Low gestational weight gain and risk of adverse perinatal outcomes in obese and severely obese women. Epidemiology 2016; 27 (06) 894-902
    CrossrefPubMedSearch in Google Scholar
  • 60 Xu Z, Wen Z, Zhou Y, Li D, Luo Z. Inadequate weight gain in obese women and the risk of small for gestational age (SGA): a systematic review and meta-analysis. J Matern Fetal Neonatal Med 2017; 30 (03) 357-367
    CrossrefPubMedSearch in Google Scholar